1887

Abstract

Mannoside phosphorylases are involved in the intracellular metabolization of mannooligosaccharides, and are also useful enzymes for the synthesis of oligosaccharides. They are found in glycoside hydrolase family GH130. Here we report on an analysis of 6308 GH130 sequences, including 4714 from the human, bovine, porcine and murine microbiomes. Using sequence similarity networks, we divided the diversity of sequences into 15 mostly isofunctional meta-nodes; of these, 9 contained no experimentally characterized member. By examining the multiple sequence alignments in each meta-node, we predicted the determinants of the phosphorolytic mechanism and linkage specificity. We thus hypothesized that eight uncharacterized meta-nodes would be phosphorylases. These sequences are characterized by the absence of signal peptides and of the catalytic base. Those sequences with the conserved E/K, E/R and Y/R pairs of residues involved in substrate binding would target β-1,2-, β-1,3- and β-1,4-linked mannosyl residues, respectively. These predictions were tested by characterizing members of three of the uncharacterized meta-nodes from gut bacteria. We discovered the first known β-1,4-mannosyl-glucuronic acid phosphorylase, which targets a motif of the lipopolysaccharide O-antigen. This work uncovers a reliable strategy for the discovery of novel mannoside-phosphorylases, reveals possible interactions between gut bacteria, and identifies a biotechnological tool for the synthesis of antigenic oligosaccharides.

Funding
This study was supported by the:
  • Ao Li , China Scholarship Council
  • Gabrielle Potocki-Veronese , Agence Nationale de la Recherche , (Award ANR-16-CE20-0006, Oligomet)
  • Gabrielle Potocki-Veronese , Horizon 2020 Framework Programme , (Award LEIT‐BIO‐2015‐685474, Metafluidics)
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2020-07-15
2020-10-30
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References

  1. Li J, Jia H, Cai X, Zhong H, Feng Q et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol 2014; 32:834–841 [CrossRef]
    [Google Scholar]
  2. Xiao L, Feng Q, Liang S, Sonne SB, Xia Z et al. A catalog of the mouse gut metagenome. Nat Biotechnol 2015; 33:1103–1108 [CrossRef]
    [Google Scholar]
  3. Xiao L, Estellé J, Kiilerich P, Ramayo-Caldas Y, Xia Z et al. A reference gene catalogue of the pig gut microbiome. Nat Microbiol 2016; 1:1–6 [CrossRef]
    [Google Scholar]
  4. Li J, Zhong H, Ramayo-Caldas Y, Terrapon N, Lombard V et al. A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment. Gigascience 2020; 9: [CrossRef]
    [Google Scholar]
  5. Brett CT, Waldron KW. Physiology and Biochemistry of Plant Cell Walls Springer; 1996 p 282
    [Google Scholar]
  6. Sharma V, Ichikawa M, Freeze HH. Mannose metabolism: more than meets the eye. Biochem Biophys Res Commun 2014; 453:220–228 [CrossRef]
    [Google Scholar]
  7. Zeleznick LD, Rosen SM, Saltmarsh-Andrew M, Osborn MJ, Horecker BL. Biosynthesis of bacterial lipopolysaccharide, IV. Enzymatic incorporation of mannose, rhamnose, and galactose in a mutant strain of Salmonella typhimurium. Proc Natl Acad Sci U S A 1965; 53:207–214 [CrossRef]
    [Google Scholar]
  8. Zhang K, Beverley SM. Mannogen-ing central carbon metabolism by Leishmania. Trends Parasitol 2019; 35:947–949 [CrossRef]
    [Google Scholar]
  9. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 2014; 42:D490–D495 [CrossRef]
    [Google Scholar]
  10. Senoura T, Ito S, Taguchi H, Higa M, Hamada S et al. New microbial mannan catabolic pathway that involves a novel mannosylglucose phosphorylase. Biochem Biophys Res Commun 2011; 408:701–706 [CrossRef]
    [Google Scholar]
  11. Sernee MF, Ralton JE, Nero TL, Sobala LF, Kloehn J et al. A family of dual-activity glycosyltransferase-phosphorylases mediates mannogen turnover and virulence in Leishmania parasites. Cell Host Microbe 2019; 26:385–399 [CrossRef]
    [Google Scholar]
  12. Cuskin F, Baslé A, Ladevèze S, Day AM, Gilbert HJ et al. The GH130 Family of Mannoside Phosphorylases Contains Glycoside Hydrolases That Target β-1,2-Mannosidic Linkages in Candida Mannan. J. Biol. Chem. 2015; 290:25023–25033 [CrossRef]
    [Google Scholar]
  13. Nihira T, Chiku K, Suzuki E, Nishimoto M, Fushinobu S et al. An inverting β-1,2-mannosidase belonging to glycoside hydrolase family 130 from Dyadobacter fermentans . FEBS Lett 2015; 589:3604–3610 [CrossRef]
    [Google Scholar]
  14. Kawahara R, Saburi W, Odaka R, Taguchi H, Ito S et al. Metabolic mechanism of mannan in a ruminal bacterium, Ruminococcus albus, involving two mannoside phosphorylases and cellobiose 2-epimerase; discovery of a new carbohydrate phosphorylase, β-1,4-mannooligosaccharide phosphorylase. J Biol Chem 2012; 287:42389–42399
    [Google Scholar]
  15. Chekan JR, Kwon IH, Agarwal V, Dodd D, Revindran V et al. Structural and Biochemical Basis for Mannan Utilization by Caldanaerobius polysaccharolyticus Strain ATCC BAA-17. J Biol Chem 2014; 289:34965–34977 [CrossRef]
    [Google Scholar]
  16. Ye Y, Saburi W, Odaka R, Kato K, Sakurai N et al. Structural insights into the difference in substrate recognition of two mannoside phosphorylases from two GH130 subfamilies. FEBS Lett 2016; 590:828–837 [CrossRef]
    [Google Scholar]
  17. La Rosa SL, Leth ML, Michalak L, Hansen ME, Pudlo NA et al. The human gut firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans. Nat Commun 2019; 10:1–14 [CrossRef]
    [Google Scholar]
  18. Grimaud F, Pizzut-Serin S, Tarquis L, Ladevèze S, Morel S et al. In Vitro Synthesis and Crystallization of β-1,4-Mannan. Biomacromolecules 2019; 20:846–853 [CrossRef]
    [Google Scholar]
  19. Nihira T, Suzuki E, Kitaoka M, Nishimoto M, Ohtsubo Ken'ichi, Ohtsubo K et al. Discovery of β-1,4-d-Mannosyl- N -acetyl-d-glucosamine Phosphorylase Involved in the Metabolism of N -Glycans. J. Biol. Chem. 2013; 288:27366–27374 [CrossRef]
    [Google Scholar]
  20. Ladevèze S, Tarquis L, Cecchini DA, Bercovici J, André I et al. Role of glycoside-phosphorylases in mannose foraging by human gut bacteria. J Biol Chem 2013; 483628:jbc.M113
    [Google Scholar]
  21. Chiku K, Nihira T, Suzuki E, Nishimoto M, Kitaoka M et al. Discovery of two β-1,2-mannoside phosphorylases showing different chain-length specificities from Thermoanaerobacter sp. X-514. PLoS One 2014; 9:e114882 [CrossRef]
    [Google Scholar]
  22. Tsuda T, Nihira T, Chiku K, Suzuki E, Arakawa T et al. Characterization and crystal structure determination of β-1,2-mannobiose phosphorylase from Listeria innocua . FEBS Lett 2015; 589:3816–3821 [CrossRef]
    [Google Scholar]
  23. Awad FN, Laborda P, Wang M, AM L, Li Q et al. Discovery and biochemical characterization of a mannose phosphorylase catalyzing the synthesis of novel β-1,3-mannosides. BBA-Gen Subjects 1861; 2017:3231–3237
    [Google Scholar]
  24. Tang S-L, Pohl NLB. Automated solution-phase synthesis of β-1,4-mannuronate and β-1,4-mannan. Org Lett 2015; 17:2642–2645 [CrossRef]
    [Google Scholar]
  25. Gerlt JA, Bouvier JT, Davidson DB, Imker HJ, Sadkhin B et al. Enzyme function Initiative-Enzyme similarity tool (EFI-EST): a web tool for generating protein sequence similarity networks. BBA-Proteins Proteom 1854; 2015:1019–1037
    [Google Scholar]
  26. Atkinson HJ, Morris JH, Ferrin TE, Babbitt PC. Using sequence similarity networks for visualization of relationships across diverse protein superfamilies. PLoS One 2009; 4:e4345 [CrossRef]
    [Google Scholar]
  27. Levin BJ, Huang YY, Peck SC, Wei Y, Martínez-del Campo A et al. A prominent glycyl radical enzyme in human gut microbiomes metabolizes trans -4-hydroxy-l-proline. Science 2017; 355:eaai8386 [CrossRef]
    [Google Scholar]
  28. Viborg AH, Terrapon N, Lombard V, Michel G, Czjzek M et al. A subfamily roadmap of the evolutionarily diverse glycoside hydrolase family 16 (GH16). J. Biol. Chem. 2019; 294:15973–15986 [CrossRef]
    [Google Scholar]
  29. Ladevèze S, Laville E, Despres J, Mosoni P, Potocki-Véronèse G. Mannoside recognition and degradation by bacteria. Biol Rev 2017; 92:1969–1990 [CrossRef]
    [Google Scholar]
  30. Svartström O, Alneberg J, Terrapon N, Lombard V, de Bruijn I et al. Ninety-nine de novo assembled genomes from the moose (Alces alces) rumen microbiome provide new insights into microbial plant biomass degradation. Isme J 2017; 11:2538–2551 [CrossRef][PubMed]
    [Google Scholar]
  31. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [CrossRef]
    [Google Scholar]
  32. Shannon P et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13:2498–2504 [CrossRef]
    [Google Scholar]
  33. Huang Y, Niu B, Gao Y, Fu L, Li W. CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 2010; 26:680–682 [CrossRef]
    [Google Scholar]
  34. Konagurthu AS, Whisstock JC, Stuckey PJ, Lesk AM. MUSTANG: a multiple structural alignment algorithm. Proteins 2006; 64:559–574 [CrossRef]
    [Google Scholar]
  35. Nakae S, Ito S, Higa M, Senoura T, Wasaki J et al. Structure of novel enzyme in mannan biodegradation process 4-O-β-D-mannosyl-D-glucose phosphorylase MGP. J Mol Biol 2013; 425:4468–4478 [CrossRef]
    [Google Scholar]
  36. Ladevèze S, Cioci G, Roblin P, Mourey L, Tranier S et al. Structural bases for N-glycan processing by mannoside phosphorylase. Acta Crystallogr D 2015; 71:1335–1346 [CrossRef]
    [Google Scholar]
  37. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [CrossRef]
    [Google Scholar]
  38. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425
    [Google Scholar]
  39. Letunic I, Bork P. Interactive tree of life (iTOL) V3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [CrossRef]
    [Google Scholar]
  40. Nielsen H. Predicting secretory proteins with SignalP. Protein Function Prediction Springer; 2017 pp 59–73
    [Google Scholar]
  41. Gawronski JD, Benson DR. Microtiter assay for glutamine synthetase biosynthetic activity using inorganic phosphate detection. Anal Biochem 2004; 327:114–118 [CrossRef]
    [Google Scholar]
  42. De Groeve MRM, Tran GH, Van Hoorebeke A, Stout J, Desmet T et al. Development and application of a screening assay for glycoside phosphorylases. Anal Biochem 2010; 401:162–167 [CrossRef]
    [Google Scholar]
  43. Macdonald SS, Armstrong Z, Morgan-Lang C, Osowiecka M, Robinson K et al. Development and application of a high-throughput functional metagenomic screen for glycoside phosphorylases. Cell Chem Biol 2019; 26:1001–1012 [CrossRef]
    [Google Scholar]
  44. Niedermeyer THJ, Strohalm M. mMass as a software tool for the annotation of cyclic peptide tandem mass spectra. PLoS One 2012; 7:e44913 [CrossRef]
    [Google Scholar]
  45. Domon B, Costello CE. A systematic Nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconj J 1988; 5:397–409 [CrossRef]
    [Google Scholar]
  46. Wildberger P, Todea A, Nidetzky B. Probing enzyme–substrate interactions at the catalytic subsite of Leuconostoc mesenteroides sucrose phosphorylase with site-directed mutagenesis: the roles of Asp49 and Arg395. Biocatal Biotransfor 2012; 30:326–337 [CrossRef]
    [Google Scholar]
  47. Lee HH, Lee JS, Cho JY, Kim YE, Hong EK. Structural characteristics of immunostimulating polysaccharides from Lentinus edodes. J Microbiol Biotechnol 2009; 19:455–461 [CrossRef]
    [Google Scholar]
  48. Guo S, Mao W, Han Y, Zhang X, Yang C et al. Structural characteristics and antioxidant activities of the extracellular polysaccharides produced by marine bacterium Edwardsiella tarda. Bioresour Technol 2010; 101:4729–4732 [CrossRef]
    [Google Scholar]
  49. Shibata N, Kobayashi H, Okawa Y, Suzuki S. Existence of novel beta-1,2 linkage-containing side chain in the mannan of Candida lusitaniae, antigenically related to Candida albicans serotype a. Eur J Biochem 2003; 270:2565–2575 [CrossRef]
    [Google Scholar]
  50. Mille C, Bobrowicz P, Trinel P-A, Li H, Maes E et al. Identification of a New family of genes involved in β-1,2-mannosylation of glycans in Pichia pastoris and Candida albicans . J Biol Chem 2008; 283:9724–9736 [CrossRef]
    [Google Scholar]
  51. Katzenellenbogen E, Kocharova NA, Toukach PV, Górska S, Korzeniowska-Kowal A et al. Structure of an abequose-containing O-polysaccharide from Citrobacter freundii O22 strain PCM 1555. Carbohydr Res 2009; 344:1724–1728 [CrossRef]
    [Google Scholar]
  52. Liu B, Knirel YA, Feng L, Perepelov AV, Senchenkova Sof'ya N. et al. Structural diversity in Salmonella O antigens and its genetic basis. FEMS Microbiol Rev 2014; 38:56–89 [CrossRef]
    [Google Scholar]
  53. Sims IM, Bacic A. Extracellular polysaccharides from suspension cultures of Nicotiana plumbaginifolia. Phytochemistry 1995; 38:1397–1405 [CrossRef]
    [Google Scholar]
  54. Alberta MJ, Holme T, Lindberg B, Lindberg J, Mosihuzzaman M et al. Structural studies of the Shigella boydii type 5 O-antigen polysaccharide. Carbohydr Res 1994; 265:121–127 [CrossRef]
    [Google Scholar]
  55. Lima IFN, Havt A, Lima AAM. Update on molecular epidemiology of Shigella infection. Curr Opin Gastroen 2015; 31:30–37 [CrossRef]
    [Google Scholar]
  56. Chen Y, Li X-H, Zhou L-Y, Li W, Liu L et al. Structural elucidation of three antioxidative polysaccharides from Tricholoma lobayense. Carbohydr Polym 2017; 157:484–492 [CrossRef][PubMed]
    [Google Scholar]
  57. Kocharova NA, Knirel YA, Shashkov AS, Kochetkov NK, Pier GB. Structure of an extracellular cross-reactive polysaccharide from Pseudomonas aeruginosa immunotype 4. J Biol Chem 1988; 263:11291–11295
    [Google Scholar]
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